[en] BACKGROUND: There is growing interest in the use of probiotics in periodontal therapy; however, until now, most research has focused on lactobacilli probiotics. The aim of this study is to evaluate the effect of 4-week use of yogurt supplemented with Bifidobacterium animalis subsp. lactis DN-173010 versus a placebo yogurt, followed by a 5-day non-brushing period. METHODS: Individuals were included in this single-mask, randomized, controlled study if probing depth (PD) was ≤3 mm and attachment loss was ≤2 mm. After professional prophylaxis, they were randomized into two groups receiving yogurt containing either placebo or B. animalis for 28 days, followed by a 5-day non-brushing period. Outcome measures were plaque index (PI), gingival index (GI), bleeding on probing (BOP), PD, gingival crevicular fluid (GCF) volume, and total amount and concentration of interleukin (IL)-1β in GCF. These were measured at baseline, after 28 days of study product use, and subsequently after 5 days of plaque accumulation. RESULTS: Fifty-one patients were analyzed. No intergroup differences could be detected before and after intake of study products. However, after plaque accumulation, significantly better results for all parameters were seen in the probiotic group compared with the control group (P <0.001): lower PI and GI, less BOP, less increase in GCF volume, and lower IL-1β total amount/concentration. CONCLUSION: The use of a probiotic yogurt supplemented with B. animalis can have a positive effect on plaque accumulation and gingival inflammatory parameters after refraining from oral hygiene practices.
Research Center/Unit :
d‐BRU - Dental Biomaterials Research Unit - ULiège
Disciplines :
Dentistry & oral medicine
Author, co-author :
Kuru, Bahar Eren; Department of Periodontology, School of Dentistry, Marmara University, Istanbul, ; Department of Periodontology, School of Dentistry, Yeditepe University, Istanbul,
Laleman, Isabelle ; Centre Hospitalier Universitaire de Liège - CHU > > Service de parodontologie, chirurgie bucco-dentaire et chirurgie implantaire ; Department of Oral Health Sciences, KU Leuven Dentistry, University Hospitals
Yalnızoğlu, Tuğçe; Department of Periodontology, School of Dentistry, Marmara University, Istanbul,
Kuru, Leyla; Department of Periodontology, School of Dentistry, Marmara University, Istanbul,
Teughels, Wim; Department of Oral Health Sciences, KU Leuven Dentistry, University Hospitals
Language :
English
Title :
The Influence of a Bifidobacterium animalis Probiotic on Gingival Health: A Randomized Controlled Clinical Trial.
WHO. Working Group Report21.PDF - Probiotic- guidelines.pdf. Available at: http://who.int/foodsafety/fs-management/en/probiotic-guidelines.pdf. Accessed January 19, 2016.
Näse L, Hatakka K, Savilahti E, et al. Effect of longterm consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res 2001;35:412-420.
Slots J, Rams TE. New views on periodontal microbiota in special patient categories. J Clin Periodontol 1991; 18:411-420.
Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: Current concepts. J Periodontol 1992;63(Suppl. 4):322-331.
Wolff L, Dahlén G, Aeppli D. Bacteria as risk markers for periodontitis. J Periodontol 1994;65(Suppl. 5):498- 510.
de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 2008;111: 1-66.
Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J 2006;30:55-60.
Riccia DN, Bizzini F, Perilli MG, et al. Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis 2007;13:376-385.
Twetman S, Derawi B, Keller M, Ekstrand K, Yucel- Lindberg T, Stecksen-Blicks C. Short-Term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand 2009;67:19-24.
Stensson M, Koch G, Coric S, et al. Oral administration of Lactobacillus reuteri during the first year of life reduces caries prevalence in the primary dentition at 9 years of age. Caries Res 2014;48:111-117.
Staab B, Eick S, Knöfler G, Jentsch H. The influence of a probiotic milk drink on the development of gingivitis: A pilot study. J Clin Periodontol 2009;36:850-856.
Karuppaiah RM, Shankar S, Raj SK, Ramesh K, Prakash R, Kruthika M. Evaluation of the efficacy of probiotics in plaque reduction and gingival health maintenance among school children -A randomized control trial. J Int Oral Health 2013;5:33-37.
Teughels W, Durukan A, Ozcelik O, Pauwels M, Quirynen M, Haytac MC. Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study. J Clin Periodontol 2013; 40:1025-1035.
Tekcxe M, Ince G, Gürsoy H, et al. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: A 1-year follow-up study. J Clin Periodontol 2015;42:363-372.
Ince G, Gürsoy H, Ipçxi SxD, Cakar G, Emekli-Alturfan E, Yilmaz S. Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol 2015;86:746-754.
Iniesta M, Herrera D, Montero E, et al. Probiotic effects of orally administered Lactobacillus reuteri-containing tablets on the subgingival and salivary microbiota in patients with gingivitis. A randomized clinical trial. J Clin Periodontol 2012;39:736-744.
Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. J Oral Microbiol 2010;2:210.3402/jom. v2i0.5344.
Ishikawa H, Aiba Y, Nakanishi M, Oh-hashi Y, Koga Y. Suppression of periodontal pathogenic bacteria in the saliva of humans by the administration of Lactobacillus salivarius TI2711. Nihon Shishubyo Gakkai Kaishi J Jpn Soc Periodontol. 2003;45:105-112.
Matsuoka T, Sugano N, Takigawa S, et al. Effect of oral Lactobacillus salivarius TI2711 (LS1) administration on periodontopathic bacteria in subgingival plaque. Nihon Shishubyo Gakkai Kaishi J Jpn Soc Periodontol 2006;48:315-324.
Vicario M, Santos A, Violant D, Nart J, Giner L. Clinical changes in periodontal subjects with the probiotic Lactobacillus reuteri Prodentis: A preliminary randomized clinical trial. Acta Odontol Scand 2013;71:813- 819.
Teughels W, Loozen G, Quirynen M. Do probiotics offer opportunities to manipulate the periodontal oralmicrobiota? J Clin Periodontol 2011;38(Suppl. 11):159- 177.
Toiviainen A, Jalasvuori H, Lahti E, et al. Impact of orally administered lozenges with Lactobacillus rhamnosus GG and Bifidobacterium animalis subsp. lactis BB-12 on the number of salivary mutans streptococci, amount of plaque, gingival inflammation and the oral microbiome in healthy adults. Clin Oral Investig 2015; 19:77-83.
Caglar E, Sandalli N, Twetman S, Kavaloglu S, Ergeneli S, Selvi S. Effect of yogurt with Bifidobacterium DN- 173 010 on salivary mutans streptococci and lactobacilli in young adults. Acta Odontol Scand 2005;63: 317-320.
Singh RP, Damle SG, Chawla A. Salivary mutans streptococci and lactobacilli modulations in young children on consumption of probiotic ice-cream containing Bifidobacterium lactis Bb12 and Lactobacillus acidophilus La5. Acta Odontol Scand 2011;69:389-394.
Cildir SK, Germec D, Sandalli N, et al. Reduction of salivary mutans streptococci in orthodontic patients during daily consumption of yoghurt containing probiotic bacteria. Eur J Orthod 2009;31:407-411.
Nagarajappa R, Daryani H, Sharda AJ, et al. Effect of chocobar ice cream containing Bifidobacterium on salivary Streptococcus mutans and Lactobacilli: A randomised controlled trial. Oral Health Prev Dent 2015;13:213-218.
Hojo K, Mizoguchi C, Taketomo N, et al. Distribution of salivary Lactobacillus and Bifidobacterium species in periodontal health and disease. Biosci Biotechnol Biochem 2007;71:152-157.
Oliveira LF, Salvador SL, Silva PH, et al. Benefits of Bifidobacterium animalis subsp. lactis probiotic in experimental periodontitis. J Periodontol 2017;88: 197-208.
Teles R, Sakellari D, Teles F, et al. Relationships among gingival crevicular fluid biomarkers, clinical parameters of periodontal disease, and the subgingival microbiota. J Periodontol 2010;81:89-98.
Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963;21: 533-551.
Slawik S, Staufenbiel I, Schilke R, et al. Probiotics affect the clinical inflammatory parameters of experimental gingivitis in humans. Eur J Clin Nutr 2011;65:857-863.
Urbaniak GC, Plous S. Research Randomizer (version 4.0) [computer software]. Available at: https://www.randomizer.orgAccessed December 01, 2011.
Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964;22:121-135.
Kuru L, Griffiths GS, Petrie A, Olsen I. Changes in transforming growth factor-beta1 in gingival crevicular fluid following periodontal surgery. J Clin Periodontol 2004;31:527-533.
Sculean A, Chiantella GC, Windisch P, Arweiler NB, Brecx M, Gera I. Healing of intra-bony defects following treatment with a composite bovine-derived xenograft (Bio-Oss Collagen) in combination with a collagen membrane (Bio-Gide PERIO). J Clin Periodontol 2005;32:720-724.
Dinarello CA. The biology of interleukin 1 and comparison to tumor necrosis factor. Immunol Lett 1987; 16:227-231.
Marks RG, Magnusson I, Taylor M, Clouser B, Maruniak J, Clark WB. Evaluation of reliability and reproducibility of dental indices. J Clin Periodontol 1993;20:54-58.
Niederman R, Zhang J, Kashket S. Short-chain carboxylicacid- stimulated, PMN-mediated gingival inflammation. Crit Rev Oral Biol Med 1997;8:269-290.
Zhang J, Kashket S, Lingström P. Evidence for the early onset of gingival inflammation following shortterm plaque accumulation. J Clin Periodontol 2002; 29:1082-1085.
Caglar E, Kuscu OO, Selvi Kuvvetli S, Kavaloglu Cildir S, Sandalli N, Twetman S. Short-Term effect of icecream containing Bifidobacterium lactis Bb-12 on the number of salivary mutans streptococci and lactobacilli. Acta Odontol Scand 2008;66:154-158.
Zhu Y, Xiao L, Shen D, Hao Y. Competition between yogurt probiotics and periodontal pathogens in vitro. Acta Odontol Scand 2010;68:261-268.
van Essche M, Loozen G, Godts C, et al. Bacterial antagonism against periodontopathogens. J Periodontol 2013;84:801-811.
Haukioja A, Yli-Knuuttila H, Loimaranta V, et al. Oral adhesion and survival of probiotic and other lactobacilli and bifidobacteria in vitro. Oral Microbiol Immunol 2006;21:326-332.
Quirynen M, Dekeyser C, van Steenberghe D. The influence of gingival inflammation, tooth type, and timing on the rate of plaque formation. J Periodontol 1991;62:219-222.
Trombelli L, Tatakis DN, Scapoli C, Bottega S, Orlandini E, Tosi M. Modulation of clinical expression of plaque-induced gingivitis. II. Identification of "high-responder" and "low-responder" subjects. J Clin Periodontol 2004;31:239-252.
Abbas F, Van der Velden U, Hart AA, Moorer WR, Vroom TM, Scholte G. Bleeding/plaque ratio and the development of gingival inflammation. J Clin Periodontol 1986;13:774-782.
Trombelli L, Scapoli C, Calura G, Tatakis DN. Time as a factor in the identification of subjects with different susceptibility to plaque-induced gingivitis. J Clin Periodontol 2006;33:324-328.
Trombelli L, Farina R, Minenna L, Carrieri A, Scapoli C, Tatakis DN. Experimental gingivitis: Reproducibility of plaque accumulation and gingival inflammation parameters in selected populations during a repeat trial. J Clin Periodontol 2008;35:955-960.
Schulz KF, Grimes DA. Blinding in randomised trials: Hiding who got what. Lancet 2002;359:696-700.
